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The diet of brown ( brunnea) in Shamwari Game Reserve, Eastern Cape,

Authors: Brown hyaenas (Hyaena brunnea) were introduced to Shamwari Game Reserve in the 1 Kerry Slater Eastern Cape Province during 2002, but their feeding ecology is poorly understood. Feeding Konrad Muller2 observations of brown hyaena by field guides and the collection of 31 scats from the study area Affiliations: took place over an 11 month period. Standard techniques were used to analyse the scats and 1Department of identify prey items present. Ten dietary categories were identified from the scats, with a mean Environmental Sciences, of 3.2 dietary categories per scat. Large remains were found in 30 of the 31 scats, with University of South Africa, South Africa kudu being the most abundant (61.0% of scats). Overall the two methods indicated at least 14 mammal being fed on by the brown hyaena. The presence of mainly large mammal 2Shamwari Game Reserve, remains and invertebrates (in 38.7% of all scats), together with the feeding observations of Eastern Cape, South Africa mainly large by field guides, suggests that brown hyaena in Shamwari are mainly Correspondence to: scavengers and that sufficient carrion is available, thereby reducing the need for them to hunt. Kerry Slater A 52.0% occurrence of plant matter was found in the scats, suggesting that plant material is an important component of their diet. Further studies are underway to investigate the feeding Email: ecology of brown hyaena in Shamwari and surrounding areas. [email protected] Conservation implications: Comprehensive scat analysis over a number of years, monitoring Postal address: of individual movement patterns and population numbers of brown hyaena in and around Private Bag X6, Florida 1710, South Africa conservation areas will be beneficial in quantifying resource use of this species.

Dates: Received: 05 Feb. 2013 Accepted: 18 Sept. 2013 Introduction Published: 28 Feb. 2014 Investigating the diet of free-ranging provides information of resources available to and utilised by these animals, but this information is not always available to wildlife area managers How to cite this article: because of constraints on time-consuming field work. The diet of a carnivore is a reflection Slater, K. & Muller, K., 2014, ‘The diet of brown of its feeding type (specialist or opportunistic), the availability of its potential prey and its hyaenas (Hyaena brunnea) morphological, behavioural and physiological adaptations (Kok & Nel 2004). in Shamwari Game Reserve, Eastern Cape, South Africa’, Previous studies on brown hyaenas (Hyaena brunnea) have shown it to have a diverse diet and, Koedoe 56(1), Art. #1143, although primarily a scavenger of mammals, it also forages for insects, reptiles, birds and their 5 pages. http://dx.doi.org/ eggs, and plants (Burgener & Gusset 2003; Kuhn, Wiesel & Skinner 2008; Maude 2005; Mills 10.4102/koedoe.v56i1.1143 & Mills 1978; Owens & Owens 1978; Skinner 1976; Skinner & Chimimba 2005; Skinner & Van Copyright: Aarde 1981; Van der Merwe et al. 2009). Despite being generalist feeders, they appear to lean © 2014. The Authors. towards specific prey items depending on their habitat. For example, in the southern Kalahari, 58 Licensee: AOSIS different food types were identified in faecal samples (Mills & Mills 1978), but along the Namib OpenJournals. This work Desert coast, the bulk of the brown hyaena’s diet is Cape fur seals ( pusillus) (Goss is licensed under the Creative Commons 1986; Kuhn et al. 2008; Siegfried 1984; Skinner & Van Aarde 1981). Brown hyaenas are inefficient Attribution License. predators and food obtained by hunting is rare (Mills & Mills 1978). In the southern Kalahari, only 4.7% of hunting attempts were successful and those vertebrates hunted successfully made up only 4.2% of the total vertebrate diet (Mills 1978). Vertebrates hunted were also of small sizes and included birds such as korhaan (Eupodotis sp.), small mammals such as lamb (Antidorcus marsupilis), springhare ( capensis), striped polecat ( striatus) and bat- eared (Otocyon megalotis) (Mills 1990). Along the Namib coast, between 2.9% (Goss 1986) and 9.6% (Wiesel 2010) of the Cape pups eaten were killed by the brown hyaenas themselves. In areas where brown hyaena ranges overlap with agricultural lands (Skinner 1976; Skinner & Van Aarde 1981) or human settlements (Kuhn et al. 2008), remains of domestic , cats, cattle, goats, sheep, horses and donkeys (Maude 2005) have been found in their faecal scats.

Brown hyaenas are sparsely distributed over the arid and semi-arid regions of southern Africa (Mills & Hofer 1998). Owing to the shy behaviour of this , only a handful of papers report on their diet and are mainly restricted to arid areas. There is therefore generally a lack of this Read online: information in most of their distribution range. Scan this QR code with your smart phone or During the early 1990s, the Eastern Cape Province transformed large areas of agriculture to more mobile device economically viable game farming, ecotourism and conservation areas (Hayward et al. 2007). to read online. This change in land use led to numerous wildlife species being reintroduced to former domestic

http://www.koedoe.co.za doi:10.4102/koedoe.v56i1.1143 Page 2 of 5 Short Communication livestock farms. These reintroductions included large hair was removed from the slide leaving the imprint of the predator species that had historically occurred in the eastern hair’s scale on the slide. Each hair sample was placed into Cape region, with the main aim of these reintroductions the front section of a Pasteur pipette. Wax was melted and being to restore ecological integrity, conserve threatened sucked up into the pipette and then dipped into cold water species and maximise ecotourism (Hayward et al. 2007). to solidify the wax. A cross-section of the hair was made by Although translocation of large carnivores is common, there cutting the front end of the pipette into small slices with a is often very little or no post-release monitoring (Hofmeyer surgical blade. The size and shape of the medulla and cortex & Van Dyk 1998). of each cross-section, together with the scale imprints, were used to identify mammal species represented in each sample Research method and design from reference material (Keogh 1983; Maude 2005; Perrin & Campbell 1980). Samples from mammal species occurring in Study area the reserve were also used to make up a reference key (see This article describes a preliminary study on the diet of Appendix 1). Remains of insects, reptiles, fruit, bone, hair, brown hyaenas at Shamwari Game Reserve in South Africa’s feathers and any other objects were identified by manually Eastern Cape Province (33°25′40′′S, 26°05′32′′E). Shamwari sorting through the faecal scats. is approximately 25 000 ha, traversing four geological formations (i.e. Bokkeveld series shale, Witteberg quartzite, Dietary diversity (H) was calculated from the scats using

Karoo sandstone and Sundays River formations) (O’Brien the Brillouin index and the cumulative diversity (Hk) was 2004). Vegetation types in Shamwari include: Kowie Thicket, plotted against the number of scats to determine if the brown Bhisho Thornveld, Suurberg Quartzite Fynbos and Suurberg hyaenas diet had been adequately sampled (Glen & Dickman Shale Fynbos (Mucina & Rutherford 2006). Shamwari 2006). The percentage occurrence of each prey item or species in is situated in the spring-dominant rainfall region of the the total number of scats was calculated as an indication of province and receives about 550 mm of rainfall per annum (Low & Rebelo 1996; Stone, Weaver & West 1998). Permanent Feeding observations water is available in the semi-perrenial Bushman’s River that Main roads flows through the reserve for 27.6 km and there are a number Bushmans river of small earth dams. Shamwari boundary

Carnivores that have been reintroduced to Shamwari include , , lion, , African wild and brown hyaena. Historical records indicate that brown hyaenas had not been seen in the eastern Cape region since the 1960s Bushmans river (Hayward et al. 2007). During 2002, two adult male and four adult female brown hyaenas wild caught from Northern R342 Cape Province farms were reintroduced to the reserve and, N10 by 2004, an estimated population of 15 hyaenas could be N2 found in Shamwari. During 2007, seven adults and sub- adults were relocated from Shamwari to other Eastern Cape N reserves. Despite this apparent success of reintroducing 10 km brown hyaenas into Shamwari, no detailed study on their diet has been conducted. FIGURE 1: Locations of brown hyaena feeding observations by field guides in Shamwari Game Reserve, Eastern Cape Province during the study period, from Procedure April 2008 to June 2009. Data on feeding observations of brown hyaenas documented by field guides whilst out on game drives with guests were Latrine locations collected between April 2008 and June 2009 (Figure 1). These Main roads recordings included the date, species being fed on, size and Bushmans river any other related information. Thirty-one fresh faecal scats Shamwari boundary were also collected from 11 latrines throughout the study area between April 2008 and May 2009 (Figure 2). Dried scats were placed into a nylon netting envelope and rinsed with Bushmans warm water to loosen the hair and other objects trapped inside. river The scats were dissected manually and all hair samples R342 were removed. A representative sample was selected for N10 analysis by inspecting all the hairs visually from each faecal N2 scat and selecting at least one hair for each size, thickness, shape, colour and length (Maude 2005). This increased the N chances of identifying all mammal species represented by 10 km hair in each faecal sample. A scale imprint was made of each FIGURE 2: Locations of brown hyaena latrines used for faecal scat collection in hair sample by placing the hair onto a glass slide that was Shamwari Game Reserve, Eastern Cape Province during the study period, from covered with liquid gelatine. Once the gelatine had dried, the April 2008 to June 2009.

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how frequently the hyaenas fed on each dietary component 0.25 (Loveridge & Macdonald 2003). This was calculated by the number of scats containing a particular food item / total 0.20 )

number of scats × 100. The relative percentage occurrence k (number of times a specific food item was encountered / total number of occurrences of all food items × 100) indicated the 0.15 importance of each food item to the overall diet (Loveridge & Macdonald 2003). A 95% confidence interval for both the 0.10 percentage occurrence and the relative percentage occurrence were generated from 1000 bootstrap simulations (Andheria, 0.05

Karanth & Kumar 2007). (H diversity Cumulative 0.00

Results Scats collected

Eighty-one feeding observations of brown hyaenas were n = 31 scats. made by field guides during the study period (Table 1). Fifty- FIGURE 3: Species accumulation curve based on the cumulative Brillouin index seven (70.00%) of the feeding observations were of brown for brown hyaena scat samples in Shamwari Game Reserve, Eastern Cape hyaenas feeding on large mammals, of which 62.00% were of Province, South Africa. Ruminantia or Perrisodactyla. During the observations these larger items were always carried away from the carcass to be TABLE 1: Feeding observations of brown hyaenas in Shamwari Game Reserve, Eastern Cape Province, South Africa. eaten elsewhere. On one occasion, a female brown hyaena was Order or Species Percentage of feeding observed carrying a large piece of a gemsbok for over 3 km suborder observations n( = 81) during 30 min of observation. Twelve observations (14.80%) % n of brown feeding on two white rhino carcasses that Ruminantia Black wildebeest (Connochaetes gnou) 4.94 4 had been killed in a territorial dispute were made during the Impala (Aepyceros melampus) 6.17 5 study period. A giraffe that had died of natural causes was Springbok (Antidorcas marsupialis) 3.70 3 observed being fed on by brown hyaenas eight times (9.88%). Common duiker (Sylvicapra grimmia) 1.23 1 Of the total observations, 11.00% (five blesbok, one kudu and Gemsbok (Oryx gazelle) 2.47 2 three springbok) were kills that brown hyaenas had stolen Bushbuck (Tragelaphus scriptus) 1.23 1 from cheetah. Brown hyaenas were also observed to kill Blesbok (Damaliscus pygargus) 8.64 7 and eat one leopard tortoise (Geochelone pardalis) and three Giraffe (Giraffa camelopardalis) 9.88 8 angulate tortoises (Chersina angulata). Kudu (Tragelaphus strepsiceros) 8.64 7 Perissodactyla White rhinoceros (Ceratotherium simum) 14.81 12 Suiformes Warthog (Phacochoerus africanus) 4.94 4 The use of a cumulative Brillouin index (Hk) indicated that the scat sample size of 31 scats was sufficient for brown hyaenas Primates Chacma baboon (Papio ursinus) 1.23 1 (Figure 3). We found a mean of 3.2 dietary categories per (Proteles cristatus) 2.47 2 hyaena scat. Large mammal remains (> 10 kg) were found in Testudines Angulate Tortoise (Chersina angulata) 3.70 3 30 of the 31 scats and were clearly the most important dietary Leopard tortoise (Geochelone pardalis) 1.23 1 component for brown hyaenas (Table 2). Five species of large - Unidentified vertebrate remains 18.52 15 mammals were identified from the scats, with kudu being - Unidentified 6.17 5 the most frequent, representing 61.0% occurrence in the diet. Blesbok and bushbuck contributed 58.1% and 41.9% to the TABLE 2: Diet of brown hyaenas in Shamwari Game Reserve, Eastern Cape Province, South Africa, as determined by faecal scats, expressed as the brown hyaena’s diet, respectively. Plains contributed percentage occurrence and relative percentage occurrence. 29.0% and warthog 12.0% to diet. Overall, at least 14 mammal Food item Percent occurrence Relative percent species were found to be included in the hyaena’s diet, as occurrence well as a variety insects, reptiles, birds and plant material. % Range Relative % Range Bushbuck (Tragelaphus scriptus) 41.9 25.8–58.1 9.0 4.9–13.9 Discussion Blesbok (Damaliscus pygargus) 58.1 38.7–74.2 12.5 7.6–18.1 Kudu (Tragelaphus strepsiceros) 61.3 42.0–77.4 13.2 7.6–18.1 Brown hyaenas usually only hunt small mammals (Owens Plains zebra (Equus quagga) 29.0 12.9–45.2 6.3 2.8–10.4 & Owens 1978) and therefore the high number of large Warthog (Phacochoerus africanus) 12.9 3.2–25.8 2.8 0.7–5.6 mammals being observed to be eaten and the hair found Insects 38.7 19.4–54.8 8.3 4.2–13.2 in the faecal scats was more than likely indicative of these Freshwater crab 3.2 0.0–9.7 0.7 0.0–2.1 prey items having been scavenged. This study confirms Tortoise egg shell 9.7 0.0–22.6 2.1 0.0–4.8 the findings of other such studies where remains in brown Unidentified hair 58.1 41.9–74.2 12.5 7.0–18.1 hyaena scats were mainly from members of the order Unidentified feathers 6.5 0.0–16.1 1.4 0.0–3.5 Ruminantia (Burgener & Gusset 2003; Van der Merwe et al. Bone remains 83.9 71.0–96.8 18.1 11.8–25.0 2009). The low frequency of small species in this study may Plant remains 51.6 32.3–67.7 11.1 6.3–16.0 suggest that sufficient carrion is available due to the presence Plastic 9.7 0.0–22.6 2.1 0.0–4.9 of other predators in the same area as the hyaenas, thereby n = 31.

http://www.koedoe.co.za doi:10.4102/koedoe.v56i1.1143 Page 4 of 5 Short Communication reducing the need for them to hunt. Although the occurrence Hayward, M.W., Adendorff, J., O’Brien, J., Sholto–Douglas, A., Bissett, C., Moolman, L.C. et al., 2007, ‘The reintroduction of large carnivores to the Eastern Cape, of plant material found in the scats (52%) is not as high as South Africa: An assessment’, Oryx 41, 205–214. http://dx.doi.org/10.1017/ found in brown hyaenas living in arid areas (Mills & Mills S0030605307001767 Hofmeyer, M. & Van Dyk, G., 1998, ‘Cheetah introductions to two North West parks: 1978), plant material is still an important component of the Case studies from Pilanesburg National Park and Madikwe Game Reserve’, in B.L. Penzhorn (ed.), as game ranch animals, pp. 60–71, Wildlife Group of the diet for brown hyaenas in Shamwari. Invertebrates that were South African Veterinary Association, Onderstepoort. consumed were more likely ingested during feeding off Keogh, H.J., 1983, ‘A photographic reference system of the microstructure of the hair carcasses. of southern African bovids’, South African Journal of Wildlife Research 13, 89–132. Kok, O.B. & Nel, J.A.J., 2004, ‘Convergence and divergence in prey of sympatric canids and felids: Opportunism or phylogenetic constraint?’, Biological Journal of the Linnaean Society 83, 527–538. http://dx.doi.org/10.1111/j.1095- Conclusion 8312.2004.00409.x Kuhn, B.F., Wiesel, I. & Skinner, J.D., 2008, ‘Diet of brown hyaenas (Parahyaena This article represents the first documented study of the brunnea) on the Namibian coast’, Transactions of the Royal Society South Africa 63(2), 150–159. http://dx.doi.org/10.1080/00359190809519219 dietary habits of brown hyaenas in Shamwari Game Reserve Loveridge, A.J. & Macdonald, D.W., 2003, ‘Niche separation in sympatric jackals ( in the Eastern Cape. Further studies are currently underway mesomelas and Canis adustus)’, Journal of Zoology, London 259, 143–153. http:// to explore the feeding ecology and the influence of apex dx.doi.org/10.1017/S0952836902003114 Low, A.B. & Rebelo, A.G., 1996, Vegetation of South Africa, Lesotho, and Swaziland, predators on the scavenging behaviour of the brown hyaenas Department of Environmental Affairs and Tourism, Pretoria. in Shamwari Game Reserve and surrounding areas. Maude, G., 2005, ‘The comparative ecology of the (Hyaena brunnea) in the Makgadikgadi National Park and a neighbouring community cattle area in ’, MSc thesis, Department of Zoology and Entomology, University of Pretoria. Acknowledgements Mills, M.G.L., 1978, ‘Foraging behaviour of the brown hyaena (Hyaena brunnea Thunberg, 1820) in the southern Kalahari’, Zeitschrift fur tierpsychologie 48, 113– We thank Shamwari Game Reserve for permission to 141. http://dx.doi.org/10.1111/j.1439-0310.1978.tb00252.x conduct the project. Nadia Muller, Dr Murray Stokoe and the Mills, M.G.L., 1990, Kalahari : The comparative behavioral ecology of two Shamwari Rangers Department assisted with logistics of the species, Chapman & Hall, London. Mills, M.G.L. & Hofer, H., 1998, Hyaenas – Status survey and conservation action plan, project. IUCN/SSC Hyaena Specialist Group, Gland. Mills, M.G.L. & Mills, E.J., 1978, ‘The diet of the brown hyaena (Hyaena brunnea) in the southern Kalahari’, Koedoe 21, 125–149. http://dx.doi.org/10.4102/koedoe. Competing interests v21i1.968 Mucina, L. & Rutherford, M.C. (eds.), 2006, ‘The vegetation of South Africa, Lesotho The authors declare that they have no financial or personal and Swaziland’, Strelitzia 19, South African National Biodiversity Institute, Pretoria. relationships that may have inappropriately influenced them O’Brien, J.W., 2004, ‘Vegetation management units of Shamwari Game Reserve’, MSc in writing this article. thesis, Terrestrial Ecology Research Unit, University of Port Elizabeth. Owens, M.J. & Owens, D.D., 1978, ‘Feeding ecology and its influence on social organization in brown hyaena (Hyaena brunnea, Thunberg) of the central Kalahari Authors’ contributions Desert’, East Africa Wildlife Journal 16, 113–135. Perrin, M.R. & Campbell, B.S., 1980, ‘Key to the mammals of the Andries Vosloo Kudu K.M. (Shamwari Game Reserve) was responsible for data Reserve (Eastern Cape) based on their hair morphology, for use in predator scat analysis’, South African Journal of Wildlife Research 10, 1–4. collection and the initial draft of the article. K.S. (University Siegfried, W.R., 1984, ‘An analysis of faecal pellets of the brown hyaena on the Namib of South Africa) was the project supervisor, analysed the data coast’, South African Journal of Zoology 19, 61. and wrote the final article. Skinner, J.D., 1976, ‘Ecology of the brown hyaena Hyaena brunnea in the Transvaal with a distribution map for southern Africa’, South African Journal of Science 72, 262–269. Skinner, J.D. & Chimimba, C.T., 2005, The mammals of the southern African subregion, References 3rd edn., Cambridge University Press, Cambridge. http://dx.doi.org/10.1017/ CBO9781107340992 Andheria, A.P., Karanth, K.U. & Kumar, N.S., 2007, ‘Diet and prey profiles of three sympatric large carnivores in Bandipur Tiger Reserve, India’, Journal of Zoology, Skinner, J.D. & Van Aarde, R.J., 1981, ‘The distribution and ecology of the brown London 273, 169–175. http://dx.doi.org/10.1111/j.1469-7998.2007.00310.x hyaena Hyaena brunnea and spotted hyaenaCrocuta crocuta in the central Namib Desert’, Madoqua 12, 231–239. Burgener, N. & Gusset, M., 2003, ‘The feeding habits of brown hyaenas (Hyaena Stone, A.W., Weaver, A.B. & West, W.O., 1998, ‘Climate and weather’, in R.A. Lubke & brunnea) on a game ranch in Limpopo Province, South Africa’, African Zoology I. DeMoor (eds.), Field guide to the eastern and southern Cape coasts, pp. 41–49, 38, 181–184. University of Cape Town Press, Cape Town. Glen, A.S. & Dickman, C.R., 2006, ‘Diet of the spotted tailed quoll (Dasyurus maculatus) Van der Merwe, I., Tambling, C.J., Thorn, M., Scott, D.M., Yarnell, R.W., Green, M. et in eastern Australia: Effects of season, sex and size’, Journal of Zoology, London al., 2009, ‘An assessment of diet overlap of two mesocarnivores in the North West 269, 241–248. Province, South Africa’, African Zoology 44(2), 288–291. Goss, R.A., 1986, ‘The influence of food source on the behavioural ecology of brown Wiesel, I., 2010, ‘Killing of Cape fur seal (Arctocephalus pusillus pusillus) pups by hyena in the Namib Desert’, MSc thesis, Department of Zoology and Entomology, brown hyenas (Parahyaena brunnea) at mainland breeding colonies along the University of Pretoria. coastal Namib Desert’, Acta Ethologica 13, 93–100.

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Appendix 1

APPENDIX 1: Animal species other than brown hyaena that occur on Shamwari APPENDIX 1 (Continues...):Animal species other than brown hyaena that occur Game Reserve. on Shamwari Game Reserve. Mammals Impala (Aepyceros melampus) Aardvark (Orycteropus afer) Kudu (Tragelaphus strepsiceros) Aardwolf (Proteles cristatus) Large-spotted (Genetta tigrina) African wild cat ( silvestris) Leopard ( pardus) (Lycaon pictus) Lion (Panthera leo) Bat-eared fox (Otocyon megalotis) Mountain reedbuck (Redunca fulvorufula) Black footed cat (Felis nigripes) Plains zebra (Equus quagga) Black rhinoceros (Diceros bicornis) Porcupine (Hystrix africaeaustralis) Black wildebeest (Connochaetes gnou) Red hartebeest (Alcelaphus buselaphus) Black-backed jackal (Canis mesomelas) Rock hyrax (Procavia capensis) Blesbok (Damaliscus pygargus) Scrub hare (Lepus saxatilis) Blue duiker (Philantomba monticola) Serval (Leptailurus serval) Buffalo (Syncerus caffer) Small grey ( pulverulenta) Bushbuck (Tragelaphus scriptus) Small-spotted genet (Genetta genetta) Bushpig (Potamochoerus larvatus) Springbok (Antidorcas marsupialis) Cape clawless ( capensis) Springhare (Pedetes capensis) Cape fox ( chama) Steenbok (Raphicerus campestris) Cape grysbok (Raphicerus melanotis) Striped polecat (Ictonyx striatus) Cape hare (Lepus capensis) Striped (Poecilogale albinucha) (Caracal caracal) Suricate (Suricata suricatta) Chacma baboon (Papio ursinus) Vervet monkey (Cercopithecus pygerythrus) Cheetah ( jubatus) Warthog (Phacochoerus africanus) Common duiker (Sylvicapra grimmia) Water mongoose (Atilax paludinosus) Eland (Tragelaphus oryx) Waterbuck (Kobus ellipsiprymnus) Elephant (Loxodonta africana) White rhinoceros (Ceratotherium simum) Gemsbok (Oryx gazella) (Cynictis penicillata) Giraffe (Giraffa camelopardalis) Reptiles Hedgehog (Atelerix frontalis) 77 species Hippopotamus (Hippopotamus amphibious) Tortoise Honey (Mellivora capensis) 4 species Appendix 1 continues →

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